Pathogen genetic control of transcriptome variation in the Arabidopsis thaliana – Botrytis cinerea pathosystem

Abstract

Disease symptoms arise from the interaction of the host and pathogen genomes. However, little is known about how genetic variation in the interaction modulates both organisms' transcriptomes, especially in polygenic interactions like those between generalist pathogens and their plant hosts. To begin mapping how polygenic pathogen variation influences both organisms' transcriptomes, we used the Botrytis cinerea -Arabidopsis thaliana pathosystem.We measured the co-transcriptome across a genotyped and genetically diverse collection of 96 B. cinerea isolates infected on the Arabidopsis wildtype, Col-0. Using the B. cinerea genomic variation, we performed genome-wide association (GWA) for each of 23,947 measurable transcripts in the host, and 9,267 measurable transcripts in the pathogen. Unlike other eGWA studies, there was a relative absence of cis-eQTL that is likely explained by structural variants and allelic heterogeneity within the pathogen's genome. This analysis identified mostly trans-eQTL in the pathogen with eQTL hotspots dispersed across the pathogen genome that altered the pathogen's transcripts, the host's transcripts, or both the pathogen and the host. Gene membership in the trans-eQTL hotspots suggests links to several known and many novel virulence mechanisms in the plant-pathogen interaction. Genes annotated to these hotspots provide potential targets for blocking manipulation of the host response by this ubiquitous generalist pathogen. This shows that genetic control over the co-transcriptome is polygenic, similar to the virulence outcome in the interaction of Botrytis cinerea on Arabidopsis thaliana.

Plant–necrotroph co-transcriptome networks illuminate a metabolic battlefield

“…The genes that did show a loss of expression across all host genotypes within a strain (i.e. BOT and BOA genes) were frequently linked to whole gene deletions that abolished their expression (Soltis et al, 2019). Thus, while there are likely some sequence variation associated expression errors, they are not a dominant signature in the data.…”

Plant nitrogen supply affects the Botrytis cinerea infection process and modulates known and novel virulence factors

“…Numerous transcriptomic approaches have been undertaken in plants, including A. thaliana , infected with B. cinerea but only gene profiles of the plant or the fungus alone have been considered (Windram et al ., 2012; Blanco‐Ulate et al ., 2014; Sham et al ., 2014; Vega et al ., 2015). Two recent publications have reported a simultaneous transcriptome analysis of B. cinerea and A. thaliana in the same infected leaf tissue (Soltis et al ., 2019; Zhang et al ., 2019). In parallel, the effects of N supply on A. thaliana have been studied at the transcriptional level (Patterson et al ., 2010; Podgorska et al ., 2013).…”

Modeling quantitative interactions: the disease outcome of generalist fungal pathogen across the plant kingdom

“…Other factors such as epistasis might also impact such gene networks and their interactions. The cross-kingdom genetic interactions have been shown through crosskingdom gene expression networks (Zhang et al2019), the existence of loci in the pathogen genome controlling gene expression of both host and pathogen (Soltis et al 2020) and also through RNA interference (Weiberg et al 2013). To understand quantitative interactions, large-scale genomic studies are needed to reveal how conserved and predictable are those networks interactions.…”

“…In Arabidopsis, resistance genes accounted only a small proportion of candidate genes that were connected to disease resistance, signaling, reactive oxygen species and other developmental processes such as light signal transduction (Corwin et al 2016;Fordyce et al 2018). In B.cinerea , genes part of networks associated with vesicular transport, degradation enzymes, metabolism and cellular processes are frequently identified (Soltis et al 2019;Soltis et al 2020;Zhang et al 2019).…”